Evolution of Signal Diversity

A paper describing this discovery (Gallant et al, 2011) has been published in the Journal of Comparative Physiology A (see publications).

Electric organs are a collection of 50-100 individual cells, termed electrocytes.  A three-dimensional reconstruction of one such electrocyte is shown above from the mormyrid Paramormyrops kingsleyeae. These cells are about 1mm in diameter, and several hundred microns thick.  In most mormyrids, the anatomy of electrocytes is identical across all electrocytes within an individual.

It is the synchronous discharge of these electrocytes that produces the electric organ discharge (EOD). There are essentially two “types” of electrocytes in mormyrids:  penetrating with anterior (Pa) innervation, and and non-penetrating with posterior innervation (NPp).  These differences in EO archetectiure contribute to the presence or absence of a single phase (P0) in the EOD, which was explained by Bennett (1961; see figure on right).  This morphological feature is of large importance in mormyrids:  current phylogenetic hypotheses suggest that Pa electrocytes originated early in the evolution of mormyrids, but then reverted in several lineages to NPp type electrocytes.  Thus, there is a major morphological correlate to the signal diversity we observe in mormyrids.

I have lately been studying a unique pattern of geographic variation, specifically in this character, in the species Paramormyrops kingsleaye. Our analysis includes histological analysis of electric organs and multivariate landmark analysis of 544 EOD signals collected from 12 localities across Gabon 1998-2009, with the most recent trip occurring in August, 2009.

In this fish, we see that peak P0 magnitude is bimodally distributed for all examined EODs, corresponding to P0-present and P0-absent individuals. P0-present EODs, the ancestral EOD type for the Paramormyrops genus, is correlated with the presence of penetrating-stalked (Pa) electrocytes in the electric organ while its magnitude is correlated with the number of penetrating stalks.  The resulting histogram of all 544 recorded EOD signals is shown on the right. We we were able to classify the signals (red, P0-present; green, P0-absent) based on a minimum between the two peaks of the histogram.  As you can see, there is no correlation with sex or size/age of the specimen.  We applied this classification scheme to each of our collecting localities, shown in the map to the left

P0-absent EODs were associated with non-penetrating posteriorly innervated electrocytes (NPp) and occurred only in two regions (one is in the North of Gabon, not shown in this map), isolated from other populations by physical barriers. In one case, this was a 30-foot waterfall, the other was a costal stream separated from adjacent streams by the Atlantic Ocean.  This, and other waterfalls in the region, has been demonstrated to be important in genetic dispersal over this area by Arnegard et al., 2005.  We are currently in the process of assessing the degree of admixture between these populations using DNA genotyping.

You might notice in the map that, at two sites along an assumed watershed boundary between P0-absent and P0-present regions isolated by the waterfall, both signaling phenotypes were collected in sympatry. In no other locations were these signal types found in sympatry across Gabon.  We analyzed the anatomy of individuals from this location.  To the right shows confocal reconstructions of the anterior and posterior faces from two electrocytes dissected from the same individual– clearly there are Pa and NPP electrocytes within the same individual.   This phenomenon of mixed morphology has never been reported for a Mormyrid fish!  Clearly, something interesting may be going on in Bambomo and Apassa creeks where individuals may be able to “circumvent” the waterfall due to flooded headwaters during the rainy season.

Why are we interested in this? The absence of penetrating stalks (and P0-absent EODs) have evolved several times in Mormyrids (current estimates suggest seven of such reversions from an early Patype!). Additionally, within the genus Paramormyrops , several independent reversions may have also taken place. We suppose that these reversions, along with our this data regarding EOD variation in Paramormyorps kingsleyae, are evidence of microevolutionary processes (reproductive isolation due to physical barriers, and potential drift or local selection) that contribute to critically important macroevolutionary changes in mormyrid signal evolution.  We take this to suggest that the developmental/genetic mechanisms underlying signal evolution may in fact be very simple!

Our next steps in this project are underway:  we are in the process of assessing the genetic structure among Paramormyrops kingsleyae within this river system using microsatellite genotyping.  We are also currently in the process of trying to identify potential candidate genes for these (and other signal differences in Paramormyrops) using subtractive hybridization.